Biological Conservation 181 (2015) 111–123
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Biological Conservation
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Review The ecological significance of giant clams in coral reef ecosystems ⇑ Mei Lin Neo a,b, William Eckman a, Kareen Vicentuan a,b, Serena L.-M. Teo b, Peter A. Todd a, a Experimental Marine Ecology Laboratory, Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, Singapore b Tropical Marine Science Institute, National University of Singapore, 18 Kent Ridge Road, Singapore 119227, Singapore article info abstract
Article history: Giant clams (Hippopus and Tridacna species) are thought to play various ecological roles in coral reef Received 14 May 2014 ecosystems, but most of these have not previously been quantified. Using data from the literature and Received in revised form 29 October 2014 our own studies we elucidate the ecological functions of giant clams. We show how their tissues are food Accepted 2 November 2014 for a wide array of predators and scavengers, while their discharges of live zooxanthellae, faeces, and Available online 5 December 2014 gametes are eaten by opportunistic feeders. The shells of giant clams provide substrate for colonization by epibionts, while commensal and ectoparasitic organisms live within their mantle cavities. Giant clams Keywords: increase the topographic heterogeneity of the reef, act as reservoirs of zooxanthellae (Symbiodinium spp.), Carbonate budgets and also potentially counteract eutrophication via water filtering. Finally, dense populations of giant Conservation Epibiota clams produce large quantities of calcium carbonate shell material that are eventually incorporated into Eutrophication the reef framework. Unfortunately, giant clams are under great pressure from overfishing and extirpa- Giant clams tions are likely to be detrimental to coral reefs. A greater understanding of the numerous contributions Hippopus giant clams provide will reinforce the case for their conservation. Tridacna Ó 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license Zooxanthellae (http://creativecommons.org/licenses/by-nc-nd/3.0/).
Contents
1. Introduction ...... 112 2. Methods ...... 112 2.1. Literature survey ...... 112 2.2. Population estimates of ecologically relevant parameters ...... 112 3. Giant clams as food ...... 114 3.1. Productivity and biomass ...... 114 3.2. Food for predators and scavengers...... 115 3.3. Expelled materials...... 115 4. Giant clams as shelter ...... 117 4.1. Shelters for coral reef fish...... 117 4.2. Shell surfaces for epibionts...... 117 4.3. Hosts for ectoparasites ...... 118 4.4. Hosts for commensals ...... 118 5. Reef-scale contributions of giant clams ...... 118 5.1. Contributors of carbonate ...... 118 5.2. Bioeroders ...... 118 5.3. Topographic enhancement ...... 118 5.4. Source of zooxanthellae (Symbiodinium spp.) ...... 119 5.5. Counteractors of eutrophication...... 120 6. Conclusion ...... 120
⇑ Corresponding author. Tel.: +65 65161034. E-mail addresses: [email protected] (M.L. Neo), [email protected] (P.A. Todd). http://dx.doi.org/10.1016/j.biocon.2014.11.004 0006-3207/Ó 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/). 112 M.L. Neo et al. / Biological Conservation 181 (2015) 111–123
Acknowledgements ...... 121 Appendix A. Supplementary material ...... 121 References ...... 121
1. Introduction however, stocks are declining rapidly in many countries (bin Othman et al., 2010; Andréfouët et al., 2013) and extirpations are As recently summarized by Bridge et al. (2013, p.528) coral occurring (Kinch and Teitelbaum, 2010; Neo and Todd, 2012, reefs globally are ‘‘suffering death by a thousand cuts’’. Some of 2013). these, including global warming and ocean acidification, are There exists a substantial body of work on the biology and notorious and possibly fatal. Others, such as the loss of particular mariculture of giant clams, but their significance in the coral reef species or genera, are generally less pernicious and do not garner ecosystem is not well understood. Some previous researchers have the same attention. Of course, all reef organisms have a role to play provided anecdotal insights into their likely roles, i.e. as food, as but giant clams (Cardiidae: Tridacninae), by virtue of their sheer shelter, and as reef-builders and shapers. For example, Mercier size (Yonge, 1975), well developed symbiosis with zooxanthellae and Hamel (1996, p.113) remarked: ‘‘Tridacna face many dangers. (Yonge, 1980), and highly threatened status throughout much of They are most vulnerable early in their life cycle, when they are prey their geographic range (Lucas, 1994), perhaps deserve special con- to crabs, lobsters, wrasses, pufferfish, and eagle rays.’’ In a popular sideration. Based on fossil tridacnine taxa, these iconic inverte- science article, Mingoa-Licuanan and Gomez (2002, p.24) com- brates have been associated with corals since the late Eocene mented: ‘‘clam populations add topographic detail to the seabed (Harzhauser et al., 2008) and facies of more recent Tridacna species and serve as nurseries to various organisms... Their calcified shells are common in the upper strata of fossilized reefs (Accordi et al., are excellent substrata for sedentary organisms.’’ Finally, Hutchings 2010; Ono and Clark, 2012). Modern giant clams are only found (1986, p.245) stated: ‘‘giant clams are recognisable in early Holocene in the Indo-West Pacific (Harzhauser et al., 2008) in the area reefs and if similar densities occurred to those on recent reefs, giant bounded by southern Africa, the Red Sea, Japan, Polynesia (exclud- clams have had a considerable ongoing impact on reef morphology.’’ ing New Zealand and Hawaii), and Australia (bin Othman et al., Even though there is evidence that giant clams contribute to the 2010). There are currently 13 extant species of giant clams (see functioning of coral reefs, this has very rarely been quantified. Table 1), including two recently rediscovered: Tridacna noae (Su Cabaitan et al. (2008) represents the only study to experimentally et al., 2014; Borsa et al., 2014) and Tridacna squamosina (previously demonstrate the benefits that giant clams can have on coral reefs. known as T. costata)(Richter et al., 2008), one new species: They showed that, compared to control plots, the presence of clams Tridacna ningaloo (Penny and Willan, 2014), and an undescribed had significantly positive effects on the richness and abundance of cryptic Tridacna sp. (Huelsken et al., 2013). Tridacna maxima is fish species and various invertebrates. Here, based on existing lit- the most widespread, while Hippopus porcellanus, Tridacna mba- erature and our own observations, we examine giant clams as con- lavuana (previously known as T. tevoroa), T. ningaloo, T. noae, Trid- tributors to reef productivity, as providers of biomass to predators acna rosewateri, and T. squamosina have much more restricted and scavengers, and as nurseries and hosts for other organisms. We distributions (Rosewater, 1965; bin Othman et al., 2010; Penny also examine their reef-scale roles as calcium carbonate producers, and Willan, 2014; Su et al., 2014). Tridacna gigas is by far the largest zooxanthellae reservoirs, and counteractors of eutrophication. Our species, reaching shell lengths of over 120 cm and weights in findings lead to the conclusion that healthy populations of giant excess of 200 kg (Rosewater, 1965). Since pre-history, giant clams’ clams benefit coral reefs in ways previously underappreciated, high biomass and heavy calcified shells have made them useful to and that this knowledge should help prioritize their conservation. humans as a source of food and material (Miller, 1979; Hviding, 1993). However, as a result of habitat degradation, technological 2. Methods advances in exploitation, expanding trade networks, and demand by aquarists, giant clam numbers are declining throughout their 2.1. Literature survey range (Mingoa-Licuanan and Gomez, 2002; Kinch and Teitelbaum, 2010; bin Othman et al., 2010). In this review, we first drew upon our own archives of publica- Giant clams are especially vulnerable to stock depletion tions, proceedings, dissertations, books, manuals, technical reports, because of their late sexual maturity, sessile adult phase, and popular science magazines, and grey literature that have been col- broadcast spawning strategy (Munro, 1989; Lucas, 1994). Fertiliza- lected during more than 10 years of giant clam research. These tion success requires sufficient numbers of spawning individuals, archives (n = 481 publications) were supplemented with key-word and low densities result in reduced (or zero) recruitment and even- searches in five major literature databases, i.e. Google Scholar, tual population collapse (Braley, 1984, 1987; Neo et al., 2013). JSTOR, PubMed, ScienceDirect, and Web-of-Science. We also used Presently, all giant clam species, other than the new species, T. ‘‘snowball’’ sampling (see Lescureux and Linnell, 2014), that is, ningaloo, the recently rediscovered T. noae and T. squamosina, and we manually searched through the reference lists of the most rel- the cryptic Tridacna sp., are protected under Appendix II of the evant giant clam papers to identify (and subsequently retrieve) Convention on International Trade in Endangered Species of Wild some of the more obscure literature. Fauna and Flora (CITES) and listed in the IUCN Red List of Threa- tened Species (Table 1). Conservation efforts are ongoing 2.2. Population estimates of ecologically relevant parameters (Heslinga, 2013) including essential basic research (e.g. restocking of clams in heavily impacted coral reefs, Guest et al., 2008; effects For all the estimates described below, we first identified surveys of shade on survival and growth of juvenile clams, Adams et al., of natural giant clams that included both population density and 2013; early chemotaxis contributing to active habitat selection, size distribution (i.e. Pearson and Munro, 1991; Chantrapornsyl Dumas et al., 2014) and the development of new restocking et al., 1996; Black et al., 2011; Gilbert et al., 2006; Todd et al., techniques (Waters et al., 2013). There are also several giant clam 2009). All densities were converted to per hectare values prior to sanctuaries under legal protection, for example, in Australia (Rees the calculations. The reported size distributions did not provide et al., 2003) and French Polynesia (Andréfouët et al., 2005, 2013); individual measurements for each clam; rather they stated the Table 1 Giant clam species list (Rosewater, 1965; Richter et al., 2008; bin Othman et al., 2010; Borsa et al., 2014; Huelsken et al., 2013; Penny and Willan, 2014; Su et al., 2014) and their conservation status categories listed by the International Union for Conservation of Nature (IUCN) Red List of Threatened Species (Molluscs Specialist Group, 1996; Wells, 1996).
Species name Description Global conservation status Hippopus hippopus (Linnaeus, 1758) Species has strong radial ribbing and reddish blotches in irregular bands on shells, growing to about 40 cm. Unlike Lower risk/conservation dependent Tridacna species, Hippopus mantle does not extend over shell margins and has a narrow byssal orifice 111–123 (2015) 181 Conservation Biological / al. et Neo M.L. Hippopus porcellanus Rosewater, 1982 Species is distinguished from H. hippopus by its smoother and thinner shells, and presence of fringing tentacles at Lower risk/conservation dependent incurrent siphon, growing to approximately 40 cm Tridacna crocea Lamarck, 1819 Smallest of all clam species, reaching lengths of about 15 cm. Burrows and completely embeds into reef substrates Lower risk/least concern Tridacna derasa (Röding, 1798) Second largest species, growing up to 60 cm. Has heavy and plain shells, with no strong ribbing Vulnerable A2cd Tridacna gigas (Linnaeus, 1758) Largest of all clam species, growing to over 1 m long. Easily identified by their size and elongate, triangular projections Vulnerable A2cd of upper shell margins Tridacna maxima (Röding, 1798) Species is identified by its close-set scutes. Grows up to 35 cm. Tends to bore partially into reef substrates Lower Risk/conservation dependent Tridacna mbalavuana Ladd, 1934 Species is most like T. derasa in appearance, but distinguished by its rugose mantle, prominent guard tentacles present Vulnerable B1 + 2c (formerly T. tevoroa Lucas, Ledua, on the incurrent siphon, thinner valves, and coloured patches on shell ribbing. Can grow over 50 cm long. Restricted to Braley, 1990) Fiji and Tonga Tridacna rosewateri Sirenko and Species is most like T. squamosa in appearance, but distinguished by its thinner shell, large byssal orifice and dense Vulnerable A2cd Scarlato, 1991 scutes on primary radial folds. Only found in Mauritius, with largest specimen measured at 19.1 cm Tridacna squamosa Lamarck, 1819 Species is identified by its large, well-spaced scutes, with shell lengths up to 40 cm Lower risk/conservation dependent Tridacna ningaloo Penny and Willan, Species is most like T. maxima in appearance; weakly differentiated morphologically but strongly defined genetically. Not assessed 2014 n. sp. Holotype specimen measures 17.9 cm. Current known distribution in Western Australia, but possibly extends to Solomon Islands Tridacna noae (Röding, 1798) Species is most like T. maxima in appearance, but distinguished by its sparsely distributed hyaline organs and oval Not assessed patches with different colors bounded by white margins along mantle edge. Shell lengths between 6 and 20 cm. Overlapping distributions with T. maxima but generally in lower abundances Tridacna squamosina Sturany, 1899 Species is most like T. squamosa in appearance, but distinguished by its crowded, well-spaced scutes, asymmetrical Not assessed (formerly T. costata Roa-Quiaoit, shell, and grows up to 32 cm. Only found in the Red Sea Kochzius, Jantzen, Zibdah, Richter, 2008) Cryptic Tridacna sp. (undescribed in Recently determined as a widely distributed cryptic species; forms an evolutionarily distinct monophyletic group Not assessed Huelsken et al., 2013) 113 114 M.L. Neo et al. / Biological Conservation 181 (2015) 111–123
number of clams in a series of size brackets or ‘bins’. For the of 0.145 were used (Pearson and Munro, 1991). For T. maxima, L1 purpose of our analysis, we assumed the size of each clam in a of 27.8, K of 0.068, and t0 of 0 were used (Black et al., 2011). Once bin was equal to (minimum bin size + maximum bin size)/2. For the ages of the clams were estimated, one year was added, and the the following equations, mass and weight are in grams, and shell von Bertalanffy equation was used to predict a new shell length. length is abbreviated to SL. The previous calculations were then used to predict biomass and Standing tissue biomass calculations: for each size T. maxima, shell weight of the clams at these increased sizes, and annual bio- wet biomass was first determined using the formulae biomass = mass and shell production were assumed to be the differences
10^[(3.0434 LOG(SLcm)) 1.6026] (Gilbert et al., 2006) for clams between the estimated values on the survey date and the predicted at Tatakoto atoll and biomass = 10^[(2.9367 LOG(SLcm)) 1.5318] values one year in the future. for clams at Fangatau atoll and Ningaloo reefs (Gilbert et al., 2006) Clearance rate (CR) calculations: for T. gigas, clearance rate for a and then assumed that 5.8% of wet biomass would convert to dry single clam (l h 1) was calculated using the formula CR = 3.68 biomass (Ricciardi and Bourget, 1998). For each size T. crocea, dry (dry weight0.397), while for T. crocea the formula used was biomass was determined using the formula biomass = CR = 0.585 (dry weight0.905)(Klumpp and Griffiths, 1994). No 6 3.24 (3.23 10 ) (SLmm)(Klumpp and Griffiths, 1994), while for T. formula was available for T. maxima. The clearance rate for each 6 3.36 gigas, the formula biomass = (0.34 10 ) (SLmm) was used size class of clams was then multiplied by the number of clams (Klumpp and Griffiths, 1994). The biomass for each size class of of that size, and the multiplied values were totalled. clams was then multiplied by the number of clams of that size, and the multiplied values were totalled. Standing shell weight calculations: for each size T. maxima, total 3. Giant clams as food clam weight was determined using the formulae weight =
10^[(3.1335 LOG(SLcm)) 0.9173] for clams at Tatakoto atoll 3.1. Productivity and biomass (Gilbert et al., 2006) and weight = 10^[(3.1634 LOG(SLcm)] 0.9495) for clams at Fangatau atoll and Ningaloo reefs (Gilbert Giant clams are mixotrophic (Jantzen et al., 2008), being capa- et al., 2006) and then subtracting wet tissue weight (calculated ble of generating biomass through both primary and secondary above) to give the weight of the shell alone. For each size T. crocea, production. Primary production is controlled by the photosynthetic shell weight was determined using the formula weight = efficiency of their symbiotic photoautotrophic zooxanthellae 5 3.51 (2.05 10 ) (SLmm )(Klumpp and Griffiths, 1994), while for (Jantzen et al., 2008; Yau and Fan, 2012). Secondary production, 5 3.11 T. gigas, the formula weight = (4.76 10 ) (SLmm) was used on the other hand, is strongly influenced by the uptake rate of (Klumpp and Griffiths, 1994). The shell weight for each size class ambient dissolved inorganic carbon (DIC) via filter feeding (Jones of clams was then multiplied by the number of clams of that size, et al., 1986; Watanabe et al., 2004). The acquisition of DIC is related and the multiplied values were totalled. to clearance rates (i.e. the volume of water each clam pumps per Annual biomass and shell production calculations: to determine unit time), and therefore clam body size (Klumpp et al., 1992). To annual biomass and shell production, von Bertalanffy equations facilitate between-taxa comparisons, the net primary productivity (available for T. gigas and T. maxima, but not T. crocea) were used (NPP) from an array of reef organisms, including giant clams, is to estimate the age of each size clam from four locations presented in Fig. 1. We acknowledge that different productivity (Pearson and Munro, 1991; Black et al., 2011; Gilbert et al., measures were used across studies; however, our aim is to provide 2006). For T. gigas, growth parameter estimates: asymptotic length estimate figures for relative rates among reef organisms. The NPP 2 1 (L1) of 80, growth (K) of 0.105, and its theoretical date of ‘birth’ (t0) of the giant clams, T. maxima (28.16 g O2 m d ) and T. squamosa
2 1 Fig. 1. Maximum net primary productivity (NPP) of different reef flora and fauna, measured in terms of net oxygen production (units = g O2 m d ). NPP values are arranged from the highest to lowest producers. Standard deviation provided when available. Information extracted from: Wanders (1976), Rogers and Salesky (1981), Porter et al. (1984), Chisholm (2003), Jantzen et al. (2008), Naumann et al. (2013). M.L. Neo et al. / Biological Conservation 181 (2015) 111–123 115
Table 2 Estimates of ecologically relevant parameters of giant clam populations found per hectare of reef area (based on data extracted from the references cited in the table). DD = data deficient.
Location Population Standing Annual biomass Shell Annual shell Water Source of density biomass production weight (kg) production (kg) filtration (Lh 1) population data (individuals) (kg dry (kg dry weight) weight) Tridacna crocea Lee-Pae Island, Andaman Sea, Thailand 2,441 17 DD 391 DD 8,144 Chantrapornsyl et al. (1996) Tioman Island, Malaysia 955 4 DD 98 DD 2,115 Todd et al. (2009) Tridacna maxima Fangatau atoll, French Polynesia 381,919 878 217 89,023 23,372 DD Gilbert et al. (2006) Tatakoto atoll, French Polynesia 909,466 1,041 238 102,833 37,040 DD Gilbert et al. (2006) Ningaloo Marine Park, Western Australia 8,600 36 7 3,898 562 DD Black et al. (2011) Tridacna gigas Great Barrier Reef, Australia 432 718 14 18,839 356 28,121 Pearson and Munro (1991)
2 1 (18.14 g O2 m d ) is greater than most of the other coral reef apparent that giant clams are widely utilized food sources on coral primary producers. From the examples in Fig. 1, the NPP of T. max- reefs, with 75 known predators (Table 3). Fishes—wrasse, trigger- ima and T. squamosa are respectively 74.1 and 47.7 higher fish, and pufferfish—prey on both juvenile and adult giant clams than the lowest NPP presented—that of the hard coral (Manicina (Alcazar, 1986; Richardson, 1991; Govan, 1992b), and bite marks 2 1 sp.) (0.38 g O2 m d )—and approximately double that of the on the mantle edges of wild clams are common (Fig. 2). In maricul- relatively fast growing branching coral Acropora palmata. The ture, ectoparasitic pyramidellids and ranellids are often abundant contribution of giant clams to overall reef productivity is hence and their attacks can devastate juvenile cohorts (Perron et al., potentially very substantial, especially when populations are dense 1985; Boglio and Lucas, 1997), but they have less impact on clams (Rees et al., 2003; Andréfouët et al., 2005; Gilbert et al., 2006). on reefs, where natural predators of these ectoparasites are present It is known that cultured stocks can produce substantial bio- (Cumming and Alford, 1994; Govan, 1995). mass, e.g. 29 t ha 1 yr 1 of wet tissue biomass for T. gigas (Barker The wide array of morphological and behavioural defences et al., 1988) (estimated 1,682 kg dry weight ha 1 yr 1) and exhibited by giant clams (Soo and Todd, 2014) is also indicative 16 t ha 1 yr 1 of wet tissue biomass for T. derasa (Heslinga et al., of their importance as a food source. Giant clams and their 1984) (estimated 928 kg dry weight ha 1 yr 1). Here, we provide predators are likely to have been in an evolutionary arms race estimates of tissue biomass for natural populations of three giant for millions of years. To resist attack, tridacnines have evolved clam species (Table 2). We also estimated annual biomass produc- large body sizes (Carter, 1968), reduced byssal orifices, and heavy tion which, if the giant clam populations were in equilibrium, strong shells (Perron et al., 1985; Alcazar, 1986; Govan et al., would equal the amount of food provided to predators and scav- 1993). Neo and Todd (2011a) found that shell strength is a pheno- engers per year. Giant clams will contribute more to productivity typically plastic trait in juvenile T. squamosa, with specimens on reefs where there is recruitment of juvenile clams, as these exposed to predator effluents being harder to crush. The shell are faster-growing. In French Polynesia, the Tatakoto atoll popula- projections (called scutes) in some Tridacna species probably offer tion of T. maxima, a medium-sized species, has a high standing crop protection from crushing predators such as crabs and jawed fishes (1,041 kg dry weight ha 1) and high productivity, being capable of (Ling et al., 2008). Other defence mechanisms include aggregation producing 238 kg dry weight ha 1 yr 1 of biomass. This population of conspecifics (Huang et al., 2007), camouflage (Todd et al., 2009), is maintained by especially rapid recruitment, probably due to rapid mantle withdrawal (McMichael, 1974), and squirting of thermal variations caused by the geography of the atoll (Gilbert water from siphons (Neo and Todd, 2011b). et al., 2006). The example T. gigas population from the Great Barrier The scavenging guild is critical to nutrient recycling on coral Reef (Table 2) has a standing crop of 718 kg dry weight ha 1, but is reefs (Keable, 1995; Rassweiler and Rassweiler, 2011) and dead essentially a relict population, consisting primarily of large adult or dying giant clams will attract a variety of small invertebrate clams. The lack of younger, faster-growing T. gigas clams explains scavengers including isopods, ostracods, amphipods, leptostracans, why the annual production of new biomass is so low (14 kg dry mysids, polychaetes, and small decapods and snails (Keable, 1995). weight ha 1 yr 1). Tridacna crocea appears to contribute minimally Many of these have not been reported to prey on healthy clams; for on a per hectare basis (due to its smaller size and low population example, the muricid gastropod (Drupella rugosa) only acts as a density) in the examples provided in Table 2, but in patches of scavenger on giant clam juveniles (Perron et al., 1985). favourable habitat, T. crocea can have densities exceeding 100 clams m 2 (Hamner and Jones, 1976) and hence may be 3.3. Expelled materials important at very local scales. While we have only presented data for single species, it is possible for up to six to co-exist on the same Opportunistic feeders may consume the materials (gametes, reef (e.g. Hardy and Hardy, 1969; Rees et al., 2003), occupying dif- faeces, and pseudofaeces) expelled by giant clams (Ricard and ferent niches based on depth and substrate type. Salvat, 1977; Lucas, 1994). For example, at the Silaqui ocean nurs- ery, Bolinao, Philippines, a large school of blue sprat (Spratelloides 3.2. Food for predators and scavengers delicatulus) fed for at least three hours on the gametes released by T. gigas (Maboloc and Mingoa-Licuanan, 2011). Routine releases Predation on juvenile giant clams has been studied extensively of undigested, photosynthetically functional zooxanthellae in the (e.g. Alcazar, 1986; Perio and Belda, 1989; Govan et al., 1993), faeces (Ricard and Salvat, 1977; Trench et al., 1981) can be impor- particularly during the ocean nursery phase of mariculture tant sources of organic matter in closed or semi-closed systems, (Govan, 1992a). Heslinga and Fitt (1987) noted that adult tridac- such as the atoll lagoons in French Polynesia (Ricard and Salvat, nines appeared to be, more-or-less, immune to predation, but there 1977; Richard, 1977). Finally, giant clams faeces contain substan- have been reported attacks on mature adults (Alcazar, 1986). It is tial amounts of nutritious mucus and protein (Ricard and Salvat, 116 M.L. Neo et al. / Biological Conservation 181 (2015) 111–123
Table 3 Predators of giant clams, including those listed by Govan (1992a,b), plus new observations and additional findings from grey literature.
Predator species Method of predation Literature source(s) PORIFERA: Family Clionaidae (Boring sponges) Unknown Bore into shells, weakening shells Govan (1992b) FLATWORM: Family Turbellaria Stylochus (Imogene) matatasi Enter the clam through either the byssal orifice or inhalant siphon Newman et al. (1991,1993) Stylochus (Imogene) sp. Govan (1992a,b) Polyclad sp. 1 Govan (1992a) MOLLUSCS: Family Buccinidae (Whelks) Cantharus fumosus – Perio and Belda (1989) Family Costellariidae (Mitres) Vexillum cruentatum – Govan (1992b) V. plicarium – Richardson (1991) Family Fasciolariidae (Tulip snails) Pleuroploca trapezium Immobilize clam by clasping mantle with foot preventing valve Govan (1992b) Pleuroploca sp. closure, insert proboscis into soft tissues Alcazar (1986) Family Muricidae (Murexes) Chicoreus brunneus Drill holes into shells of juvenile clams Abdon-Naguit and Alcazar (1989), Govan (1992a,b) C. microphyllum Drill holes into shells Govan (1992a,b) C. palmarosae Often drill through valves; may attack via valve gape or byssal orifice Govan et al. (1993) C. ramosus Insert proboscis into byssal gape to reach soft tissues, inject paralytic Heslinga et al. (1984), Alcazar (1986), Govan (1992b) substance Cronia fiscella Drill holes into shells of juvenile clams Govan (1992b) C. margariticola Through valve gape Govan (1992a,b) C. ochrostoma Drill holes into shells Govan (1992b) Morula granulata Drill holes into shells Govan (1992a,b) Muricodrupa fiscella Drill holes into shells Govan (1992a) Thais aculeata Attack through valve gape Govan (1992a,b) Family Octopodidae (Octopus) Octopus sp. Chip shells; pry valves apart to feed Heslinga et al. (1984), Barker et al. (1988), Govan (1992b), Mercier and Hamel (1996) Family Pyramidellidae Turbonilla sp. Use their long, flexible proboscis to suck clams’ body fluids, either Govan (1992a,b) Tathrella iredalei from mantle edge or through byssal orifice Heslinga et al. (1990), Govan (1992b) Family Ranellidae (Tritons) Bursa granularis Insert proboscis between valves of prey Govan et al. (1993) Cymatium aquatile Injection of an immobilizing fluid through mantle or byssal orifice, Abdon-Naguit and Alcazar (1989), Govan then feed on soft tissues (1992a,b,1995) C. muricinum Perron et al. (1985), Govan (1992a,b,1995) C. nicobaricum Govan (1992a,b,1995) C. pileare Govan (1992a,b,1995) C. vespaceum Perio and Belda (1989), Govan (1992b) Family Volutidae (Volutes) Melo amphora – Loch (1991) Melo sp. – Govan (1992b) ECHINODERM Seastar Exert powerful suction and tire adductor muscles (pry open clam) Weingarten (1991) CRUSTACEANS: Family Diogenidae (Hermit crabs) Dardanus deformis Crushed 26 juvenile T. gigas in 3 days Heslinga et al. (1984) D. lagopodes Chip valve ends Govan (1992a) D. pedunculatus Crush or chip valves of prey Govan (1992a), Govan et al. (1993) Family Gonodactylidae (Mantis shrimps) Gonodactylus chiragra Smash shells Govan (1992a) Gonodactylus sp. – Govan (1992b) Family Portunidae (Swimming crabs) Thalamita admete Chip shells; attack via byssal orifice Govan (1992a) T. coerulipes Govan (1992a) T. crenata Crush shells; may pry clam open via ventral margin Ling (2007) T. danae Crush or chip valves; attack via byssal orifice of clams Govan et al. (1993) T. spinimana – Richardson (1991) T. stephensoni Chip shells; attack via byssal orifice Govan (1992a) T. cf. tenuipes Govan (1992a) Thalamita sp. Penetrate soft tissues of adults through either byssal orifice or the Alcazar (1986), Govan (1992b) inhalant siphon Family Xanthidae (Stone crabs) Atergatis floridus Crush or chip valves Richardson (1991), Govan et al. (1993) A. integerrimus Richardson (1991) Atergatis spp. Govan (1992b) Carpilius convexus Crush or chip valves of juvenile clams Alcazar (1986), Govan (1992a,b), Govan et al. (1993) C. maculatus Crush shells Govan (1992a,b) M.L. Neo et al. / Biological Conservation 181 (2015) 111–123 117
Table 3 (continued)
Predator species Method of predation Literature source(s) Demania cultripes Crush shells of juvenile clams Alcazar (1986), Govan (1992b) Leptodius sanguineus Crush shells Govan (1992a,b) Lophozozymus pictor Crush or chip shells Richardson (1991), Govan (1992b) Myomenippe hardwickii Crush shells; may attack via byssal orifice Ling (2007) Zosimus aeneus Crush shells Govan (1992a,b) FISH: Family Balistidae (Triggerfish) Balistapus undulatus Feed on mantle and the exposed byssus and foot of adult clams Alcazar (1986), Perio and Belda (1989) Balistoides viridescens Crush or chip shells Heslinga et al. (1990) Balistoides sp. Govan (1992b) Pseudobalistes flavimarginatus Heslinga et al. (1990), Chambers (2007) Pseudobalistes sp. Govan (1992b) Rhinecanthus sp. Govan (1992b) Family Lethrinidae (Emperors) Monotaxis grandoculis Directly consumed 50 juvenile T. squamosa in <2 h Heslinga et al. (1984), Govan (1992b) Family Labridae (Wrasses) Cheilinus fasciatus – Richardson (1991) Cheilinus sp. Crush or chip shells Govan (1992b) Choerodon anchorago – Richardson (1991) C. schoenleinii – Richardson (1991) Choerodon sp. Crush or chip shells Govan (1992b) Halichoeres sp. Feed only on the byssus and foot of unanchored clams Alcazar (1986), Govan (1992b) Thalassoma hardwicke – Richardson (1991) T. lunare – Richardson (1991) Family Myliobatidae (Eagle rays) Aetobatis narinari Crush shells Heslinga et al. (1990), Govan (1992b), Chambers (2007) Family Tetraodontidae (Pufferfish) Canthigaster solandri – Richardson (1991) C. valentini Crush or chip shells Perio and Belda (1989), Govan (1992b) Tetraodon stellatus Heslinga et al. (1990), Govan (1992b), Chambers (2007) TURTLES: Family Cheloniidae Caretta caretta – Bustard (1972) Chelonia mydas Break off shell flukes and ingest as calcium carbonate dietary Weingarten (1991) supplement
1977) that can make a significant dietary contribution to reef fish; be common in marine ecosystems (Harder, 2008), only a handful of the adult black damselfish (Neoglyphidodon melas), for instance studies have discussed its ecological importance (e.g. Abellö et al., (Chan, 2007). 1990; Creed, 2000; Botton, 2009). Giant clam shells have been reported to harbour a variety of burrowing (Yonge, 1955; Turner 4. Giant clams as shelter and Boss, 1962) and encrusting (Roscoe, 1962; Rosewater, 1965) reef inhabitants, although the authors of these studies did not list 4.1. Shelters for coral reef fish specific taxa. Our own observations of clam-associated epibionts include macroalgae, sponges, ascidians, nudibranchs, bryozoans, Coral reef fish diversity is related to coral cover (Bell and Galzin, tubeworms, hard and soft corals, as well as small mobile inverte- 1984; Ault and Johnson, 1998) and substrate complexity brates (Fig. 3). Some, such as macroalgae (Fatherree, 2006), boring (Gratwicke and Speight, 2005; Lingo and Szedlmayer, 2006). Dense sponges (Norton et al., 1993), the boring worm (Oenone fulgida) aggregations of giant clams can increase topographic heterogene- (Delbeek and Sprung, 1994), and pest anemones (Aiptasia spp.) ity of the seabed and serve as nurseries and shelters for fishes. A (Fatherree, 2006) can harm their tridacnine hosts. In addition, foul- restoration study in the Philippines demonstrated that T. gigas ing algae on juvenile clams can reduce growth and lead to death by introduced onto degraded reefs significantly improved fish diver- interfering with valve movement (unpublished data). Conversely, sity and abundance compared to control plots (Cabaitan et al., other epibionts may protect their hosts by contributing anti-pred- 2008). An increase in habitat relief usually facilitates recruitment ator defenses (Feiferak, 1987) and/or camouflage (Harder, 2008). and settlement of juvenile fish and helps reduce predation by pro- Vicentuan-Cabaitan et al. (2014) identified the community liv- viding refuges (Beukers and Jones, 1997; Lecchini et al., 2007) ing on the valves of T. squamosa in Singapore. They found at least while the shell ridges of giant clams represent suitable obscure 49 species belonging to a minimum of 36 families living on the surfaces for the deposition of fishes’ egg masses (Weingarten, shells of eight T. squamosa individuals (shell lengths 236– 1991). The large mantle cavities of tridacnines also afford shelter 400 mm). Vicentuan-Cabaitan et al. (2014) also highlighted that to smaller fishes, such as the pearlfish (Encheliophis homei)(Trott giant clam shells provide much more surface area for colonization and Chan, 1972) and anemone fishes in the absence of host compared to the patch of substrate they occupy (a 26:1 ratio based anemones (Arvedlund and Takemura, 2005). on three adult T. squamosa specimens). A complete taxa checklist was not provided in their short paper, but it is now included here 4.2. Shell surfaces for epibionts (Table A1). As this list is for just one tridacnine species at a single locality, we expect that it represents only a small percentage of the On coral reefs, where settlement surfaces are limiting, epibiosis taxa that live on the shells of all giant clam species (that vary in is an alternative colonization strategy for sessile organisms (Wahl size, shell morphology, habitat preference, and global distribution) and Mark, 1999; Harder, 2008). Nevertheless, while epibiosis may (see Fig. 3). 118 M.L. Neo et al. / Biological Conservation 181 (2015) 111–123
to T. gigas (Bruce, 1983, 2000). Due to their long lifespans, giant clams can host many generations of commensals and the absence of any trauma to collected examples suggests that life within tridacnines is secure (Bruce, 2000).
5. Reef-scale contributions of giant clams
5.1. Contributors of carbonate
The calcium carbonate framework of coral reefs is maintained by opposing processes of carbonate production and removal (Le Campion-Alsumard et al., 1993; Mallela and Perry, 2007). Sclerac- tinian corals are the primary carbonate producers on most tropical reefs (Hubbard et al., 1990; Vecsei, 2004), followed by calcareous algae, gastropods, bivalves, and foraminiferans (Mallela and Perry, 2007; Perry et al., 2012). Giant clams are rarely mentioned as carbonate contributors to reef frameworks, even though they have large shells, mostly made up of aragonite—a calcium carbon- ate polymorph (Moir, 1990). Shell carbonates are generally derived from ambient dissolved inorganic carbon (Romanek and Grossman, 1989), but also include carbon from metabolic respiration and zoo- xanthellae photosynthesis within the mantle tissues (Jones et al., 1986; Watanabe et al., 2004). The relict population of T. gigas from the Great Barrier Reef (Table 2) may only produce 356 kg ha 1 yr 1 of new shell material but Barker et al. (1988) estimated that a high- density cultured population of T. gigas could produce shell material in excess of 80 t ha 1 yr 1. The natural T. maxima atoll populations in French Polynesia are capable of producing 23–37 t ha 1 yr 1 (Table 2) and are so dense that they create small islands called Fig. 2. Fish bite marks on the mantle edge of (a) Tridacna crocea (shell length mapiko (Gilbert et al., 2006). 14 cm) from Tioman Island, Malaysia and (b) Tridacna gigas (shell length 80 cm) from Magnetic Island, Australia. 5.2. Bioeroders 4.3. Hosts for ectoparasites Bioeroders such as grazers, etchers, and borers can increase the Various cyclopoid copepods live within giant clams (Table A2). removal rate of the reef’s carbonate framework (Clapp and Kenk, Even though they are capable of influencing the growth, fecundity, 1963; Hutchings, 1986). The boring giant clam species, T. crocea and survival of their hosts (Finley and Forrester, 2003; Johnson (Hamner and Jones, 1976) and, to a lesser extent, T. maxima et al., 2004), the biology of these cyclopoids is poorly understood. (Yonge, 1980; Hutchings, 1986), are usually found embedded in Anthessius and Lichomolgus are usually found inside the mantle either dead coral heads or dead patches of live colonies (Morton, cavity (Humes, 1972, 1976), while Paclabius inhabits the pericar- 1990). Burrowing by T. crocea has been described as both a dium, i.e. the membrane enclosing the heart (Kossmann, 1877). mechanical process and chemical etching. Mechanically, T. crocea Multiple cyclopoid species have been found within the same clam enlarge their burrows by grinding back and forth within them, host (Humes, 1972, 1976). Ectoparasitic gastropods are also known and fine shell corrugations on their valves wear away at the bur- to plague giant clams (also see Section 3.2.), and are especially row walls (Yonge, 1953; Hamner and Jones, 1976). Chemical etch- severe in cultured juveniles (Cumming and Alford, 1994). ing (Hedley, 1921; Yonge, 1980) is performed by extending the pedal mantle tissue out of the byssal opening and dissolving the 4.4. Hosts for commensals substrate under and around the clam via excreted solvents (Yonge, 1980; Fatherree, 2006). Given sufficient time and numbers Bivalves host a wide diversity of commensal fauna (Blanco and of settling and growing/burrowing individuals, T. crocea will even- Ablan, 1939; De Grave, 1999), providing refuge (Rosewater, 1965) tually erode away a dead coral head (Hamner and Jones, 1976; and/or food (Fankboner, 1972). The recorded commensals for Glynn, 1997), but this erosive effect is limited to these habitats that tridacnines include pinnotherid pea crabs (Fig. 4; Table A3) and are particular to T. crocea, and does not lead to wide scale attrition pontoniinid shrimps (Fig. 5; Table A4). Pea crabs are common of the reef (Paulay and Kerr, 2001; Aline, 2008). Even though little within the mantle cavities of bivalves (Stauber, 1945; Schmitt is known about the effects of T. maxima’s burrowing, McMichael et al., 1973), positioning themselves on the ctenidial surface (gills) (1974) and Hutchings (1986) both remarked that, due to their with their strong grip and gaining access to food aggregated by the higher densities, they could contribute significantly to biological host (Stauber, 1945). Xanthasia murigera (Fig. 3) is probably the erosion on coral reefs. most widespread, being found in five clam species (Table A3). Pon- toniinid shrimps can also inhabit the mantle cavities of giant 5.3. Topographic enhancement clams. With hooked walking-leg dactyls (Fujino, 1975), they anchor themselves against the currents generated by the gills, Mollusc shells are known to influence their environments, avoiding expulsion (Fankboner, 1972). While some species are either by creating or modifying habitats for other organisms commensal to multiple tridacnine species (Table A4), Anchistus (Gutiérrez et al., 2003). Giant clams can modulate water flow and gravieri appears to be obligate to Hippopus hippopus (McNeill, fluid transport as they add topographical relief to the seabed 1953; Bruce, 1977, 1983) whilst Paranchistus armatus is restricted (Weingarten, 1991; Cabaitan et al., 2008). Depending on their M.L. Neo et al. / Biological Conservation 181 (2015) 111–123 119
Fig. 3. Epibiota diversity amongst giant clam species. (a) Tridacna gigas with a burrowing giant clam (Tridacna crocea) in its shell; Mecherchar Island, Republic of Palau, March 2011. (b) Tridacna derasa with hard coral (Favites sp.) growing on it; Ouvea island of the Loyalty Islands, New Caledonia, August 2010. (c) Hippopus sp. with encrusting crustose coralline algae; Bali, Indonesia, May 2011. (d) Tridacna maxima hosting a range of encrusting epibionts; Kumejima, Okinawa, Japan; November 2009.
Fig. 4. Commensal pinnotherids (Xanthasia murigera; ZRC2013.0790) found within the mantle cavity of a fluted giant clam (Tridacna squamosa; shell length = 150 mm). (a and b) Carapace length (CL) = 5 mm. (c and d) CL = 11.5 mm.
density, their influence on water flow can be significant. Giant clam 1998). Even after a clam’s death, their heavy valves remain and shells are expected to agitate flow boundary layers much more continue to affect water flow. than the shells of smaller bivalves (Grant et al., 1992; Pilditch et al., 1998), since flow perturbation is correlated to the heights 5.4. Source of zooxanthellae (Symbiodinium spp.) and diameters of protruding objects (Eckman and Nowell, 1984). Aggregations of giant clams are likely to further increase flow Nutrient cycling between zooxanthellae and their coral hosts is perturbation and cause turbulence eddies (Lenihan, 1999). These the key to both organisms’ success in oligotrophic coral reef envi- hydrodynamic disturbances in turn affect the rates at which trans- ronments (Muscatine and Porter, 1977) and similar cycling occurs port of particles and solutes can occur (Gutiérrez et al., 2003). For between zooxanthellae and other organisms, such as zooxanthel- instance, aggregations of bivalves have been shown to alter sedi- late jellyfish (Pitt et al., 2009). Zooxanthellae within giant clams ment transport patterns and rates (Grant et al., 1992; Lenihan, utilize the hosts’ nitrogenous waste with virtually no loss from 1999) and enhance phytoplankton down-flux (Pilditch et al., the system (Hawkins and Klumpp, 1995), meaning that they have 120 M.L. Neo et al. / Biological Conservation 181 (2015) 111–123
6. Conclusion
This review details how giant clams are effective ecosystem engineers that play multiple roles in coral reefs. Their high biomass production, coupled with their wide range of known predators, suggest that giant clams are an important food item. In addition, their gametes and faeces are food to opportunistic feeders. Due to their large shell size, giant clams can shelter reef fish as well as support a diverse and abundant array of epibionts, ectoparasites, and commensals. Furthermore, some species, such as the pontonii- nid shrimp (Paranchistus armatus), are only found in tridacnine hosts. At the reef-scale, dense populations of giant clams can annu- ally contribute 100s to 1,000s kg ha 1 of shell material to a coral reef, far outweighing localized erosion by T. crocea and T. maxima. Giant clams provide their symbiotic Symbiodinium with nutrients and protection, resulting in tridacnines acting as algal ‘reservoirs’. They also filter large volumes of water—which can potentially Fig. 5. A commensal pontoniinid (Anchistus sp.; body length = 34 mm) found counteract eutrophication. While we have only evaluated the eco- resting on the mantle of a fluted giant clam (Tridacna squamosa; shell length = 243 mm). logical roles of the more common giant clam species: H. hippopus, T. crocea, T. derasa, T. gigas, T. maxima, and T. squamosa, we expect that the rarer species perform functions similar to those of their far greater access to nitrogen than they would if living in the close relatives. surrounding seawater. Giant clams also protect their symbiotic Even though there have been numerous giant clam population zooxanthellae from predation (Fankboner, 1971) and excessive collapses (e.g. Munro, 1989; Kinch and Teitelbaum, 2010; Neo ultraviolet irradiation (Ishikura et al., 1997). and Todd, 2012), it is difficult to measure the ecosystem-level Giant clams release large numbers of zooxanthellae in their fae- effects of these events due to the concomitant impacts of multiple cal pellets. To regulate symbiont density a T. derasa can discharge stressors that typify contemporary reefs (Hughes and Connell, 4.9 105 cells clam 1 d 1 of intact zooxanthellae (Maruyama 1999). Nevertheless, some negative consequences are predictable, and Heslinga, 1997) and T. gigas can discharge 4.7 105 - for example, biomass and carbonate production, surface area for cells clam 1 d 1 (Buck et al., 2002). These are both several orders epibionts, and water filtering, are all expected to decrease with of magnitude higher than the release rates of corals (Yamashita reduced giant clam abundance. Other effects might require thresh- et al., 2011). As noted by Maruyama and Heslinga (1997, p.475), olds to be breached, for example, a minimum density of giant ‘‘most of the discharged zooxanthellae were indistinguishable from clams may be needed before they act as effective fish nurseries. intact algal cells freshly isolated from the mantle.’’ Trench et al. It is unlikely, however, that researchers would experimentally (1981) also found that zooxanthellae in faecal pellets were intact, remove clams from a healthy reef to measure the outcome. On photosynthetically active, and culturable. The branched tubular the other hand, restocking programmes present an excellent system extending from a giant clam’s stomach into its mantle opportunity to monitor the response of the reef to enhanced clam (Fankboner and Reid, 1990; Norton et al., 1992) provides numerous numbers; unfortunately this is rarely done. As mentioned in the microhabitats for zooxanthellae (Norton et al., 1992) allowing mul- Introduction, the one exception is Cabaitan et al. (2008), who tiple clades or multiple types from a single clade of symbionts to specifically set out to test the localized effects of transplanting co-exist in a single host (Baillie et al., 2000; DeBoer et al., 2012). maricultured giant clams (T. gigas, >40 cm shell length) into repli- The substantial quantities and (possibly) types of zooxanthellae cate 5 5m2 plots of degraded patch reef in the Philippines (25 released from giant clams become available for other zooxanthel- clams per plot). Within three months, their ‘‘other biota’’ category late-dependent species to ‘take up’, hence contributing to the (i.e. ascidians, anemones, gorgonians, soft corals, sponges, and wider coral reef ecosystem. zoanthids) had increased significantly from 2.0% to 14.8% cover; with no change observed in the control plots. Within the same time period fish species richness and abundance also increased sig- 5.5. Counteractors of eutrophication nificantly. Similar research at different locations, and with other giant clam species and densities, is needed. In coastal marine waters, corals may be competitively excluded Any significant ecological benefits will likely only accrue where by macroalgae or heterotrophic filter feeders as the water becomes giant clams are present in healthy, i.e. self-sustaining, populations more eutrophic (Fabricius, 2005). Shallow water benthic bivalves and hence their conservation is paramount. As highlighted by Neo are known to be natural controllers of eutrophication (Officer and Todd (2013), the CITES and IUCN data for giant clams are out- et al., 1982) and giant clams can perform this function in two ways: dated and potentially misleading. Importantly, there are now three by filtering water and by sequestering nutrients (Klumpp and species recently rediscovered or undescribed, plus one entirely Griffiths, 1994). Giant clams filter large quantities of seawater; new species, that have no official conservation status (Table 1). even a sparse population of mature T. gigas (0.04 clams m 2)on Giant clams should feature more prominently when planning mar- the Great Barrier Reef is capable of filtering over 28,000 l ha 1 h 1 ine protected areas and integrated coastal management schemes (Table 2). Giant clams also clear water of algal cells efficiently, e.g. (van Wynsberge et al., 2013) and national/local assessments must Tridacna species ingest 51–58% while H. hippopus ingests 81% be part of this process. Notably, not only are giant clams useful for (Klumpp and Griffiths, 1994). Whether algal biomass is assimilated the functioning of coral reefs, they can help protect them by acting by the clams or excreted as faeces, it is removed from the water as surrogate species. Giant clams are already considered an indica- column in the short term and will therefore not contribute to tur- tor species by Reef Check (Hodgson, 2001) and, being well-known bidity. By locking assimilated nutrients away in their biomass charismatic invertebrate megafauna (for instance, fourteen cul- (Table 2), giant clams sequester them from the water where they tured T. gigas are used in snorkel trails at Magnetic Island; Braley, could otherwise encourage macroalgae to flourish. pers. comm., 2014), they have the potential to play a flagship role M.L. Neo et al. / Biological Conservation 181 (2015) 111–123 121
(sensu Walpole and Leader-Williams, 2002, but see Favreau et al., Ault, T.R., Johnson, C.R., 1998. Relationships between habitat and recruitment of 2006) in reef conservation. three species of damselfish (Pomacentridae) at Heron Reef, Great Barrier Reef. J. Exp. Mar. Biol. Ecol. 223, 145–166. We are not proposing that giant clams are essential to the Baillie, B.K., Belda-Baillie, C.A., Maruyama, T., 2000. Conspecificity and Indo-Pacific survival of coral reefs; however, there can be no doubt that they distribution of Symbiodinium genotypes (Dinophyceae) from giant clams. J. make a positive contribution to these critically important tropical Phycol. 36, 1153–1161. Barker, J.R., Crawford, C.M., Shelley, C., Braley, R.D., Lucas, J.S., Nash, W.J., Lindsay, S., ecosystems. Based on the wide range of ecological functions they 1988. Ocean-nursery technology and production data from lines and cover for perform, giant clams are unique among reef organisms and there- the giant clam, Tridacna gigas. In: Copland, J.W., Lucas, J.S. (Eds.), Giant clams in fore deserve attention. In combination with their status as the Asia and the Pacific, Australian Centre for International Agricultural Research, Canberra, Australia. Monograph No. 9, pp. 225–228. world’s largest bivalves and their popularity with SCUBA divers, a Bell, J.D., Galzin, R., 1984. Influence of live coral cover on a coral reef fish greater understanding of giant clams’ contributions will provide communities. Mar. Ecol. Prog. Ser. 15, 265–274. managers with ‘ammunition’ to justify their protection. Crucially, Beukers, J.S., Jones, G.P., 1997. Habitat complexity modifies the impact of piscivores on a coral reef fish population. Oecologia 114, 50–59. both their international and local conservation statuses need to bin Othman, A.S., Goh, G.H.S., Todd, P.A., 2010. The distribution and status of giant be updated and monitored (Brito et al., 2010; Neo and Todd, clams (family Tridacnidae) – a short review. Raffles Bull. Zool. 58, 103–111. 2013) if appropriate management strategies are to be developed. Black, R., Johnson, M.S., Prince, J., Brearley, A., Bond, T., 2011. Evidence of large, local Whatever safeguards can be established will not only boost giant variations in recruitment and mortality in the small giant clam, Tridacna maxima, at Ningaloo Marine Park, Western Australia. Mar. Freshwater Res. 62, clam populations but, by extension, also benefit coral reefs. 1318–1326. Blanco, G.J., Ablan, G.L., 1939. A rare parasitic crab new to Pangasinan Province, Acknowledgements Luzon. Philipp. J. Sci. 70, 217–219. Boglio, E.C., Lucas, J.S., 1997. 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